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Genomes of the cosmopolitan fruit pest Bactrocera dorsalis (Diptera: Tephritidae) reveal its global invasion history and thermal adaptation

Zhang Y 1 , Liu S 2 , De Meyer M 3 , Liao Z 1 , Zhao Y 1 , Virgilio M 3 Show all authors , Feng S 1 , Qin Y 1 , Singh S 4 , Wee SL 5 , Jiang F 6 , Guo S 1 , Li H 2 , Deschepper P 3 , Vanbergen S 3 , Delatte H 7 , van Sauers-Muller A 8 , Syamsudin TS 9 , Kawi AP 10 , Kasina M 11 , Badji K 12 , Said F 13 , Liu L 1 , Zhao Z 1 , Li Z 14

Affiliations 

  • 1 College of Plant Protection, China Agricultural University, Beijing 100193, China; Key Laboratory of Surveillance and Management for Plant Quarantine Pests, Ministry of Agriculture and Rural Affairs, Beijing 100193, China
  • 2 College of Plant Protection, China Agricultural University, Beijing 100193, China
  • 3 Royal Museum for Central Africa, Invertebrates Section and JEMU, Tervuren B3080, Belgium
  • 4 Department of Fruit Science, Punjab Agricultural University, Ludhiana, Punjab, India
  • 5 Centre for Insect Systematics, Department of Biological Sciences and Biotechnology, Faculty of Science and Technology, Universiti Kebangsaan Malaysia, Bangi 43600, Selangor Darul Ehsan, Malaysia
  • 6 Institute of Plant Quarantine, Chinese Academy of Inspection and Quarantine, Beijing 100176, China
  • 7 CIRAD UMR PVBMT, Ambatobe, Madagascar
  • 8 Ministry of Agriculture, Animal Husbandry and Fisheries, Paramaribo, Suriname
  • 9 School of Life Science and Technology, Bandung Institute of Technology, Bandung 40132, Indonesia
  • 10 National Agriculture Quarantine & Inspection Authority, Port Moresby, Papua New Guinea
  • 11 Apiculture Research Institute, P.O. Box 32-40302, Marigat, Kenya
  • 12 Crop Protection Directorate, Dakar, Senegal
  • 13 Department of Agriculture, Abdul Wali Khan University Mardan, Khyber Pakhtunkhwa, Mardan, Pakistan
  • 14 College of Plant Protection, China Agricultural University, Beijing 100193, China; Key Laboratory of Surveillance and Management for Plant Quarantine Pests, Ministry of Agriculture and Rural Affairs, Beijing 100193, China. Electronic address: lizh@cau.edu.cn
J Adv Res, 2023 Nov;53:61-74.
PMID: 36574947 DOI: 10.1016/j.jare.2022.12.012

Abstract

INTRODUCTION: The oriental fruit fly Bactrocera dorsalis is one of the most destructive agricultural pests worldwide, with highly debated species delimitation, origin, and global spread routes.

OBJECTIVES: Our study intended to (i) resolve the taxonomic uncertainties between B. dorsalis and B. carambolae, (ii) reveal the population structure and global invasion routes of B. dorsalis across Asia, Africa, and Oceania, and (iii) identify genomic regions that are responsible for the thermal adaptation of B. dorsalis.

METHODS: Based on a high-quality chromosome-level reference genome assembly, we explored the population relationship using a genome-scale single nucleotide polymorphism dataset generated from the resequencing data of 487 B. dorsalis genomes and 25 B. carambolae genomes. Genome-wide association studies and silencing using RNA interference were used to identify and verify the candidate genes associated with extreme thermal stress.

RESULTS: We showed that B. dorsalis originates from the Southern India region with three independent invasion and spread routes worldwide: (i) from Northern India to Northern Southeast Asia, then to Southern Southeast Asia; (ii) from Northern India to Northern Southeast Asian, then to China and Hawaii; and (iii) from Southern India toward the African mainland, then to Madagascar, which is mainly facilitated by human activities including trade and immigration. Twenty-seven genes were identified by a genome-wide association study to be associated with 11 temperature bioclimatic variables. The Cyp6a9 gene may enhance the thermal adaptation of B. dorsalis and thus boost its invasion, which tended to be upregulated at a hardening temperature of 38 °C. Functional verification using RNA interference silencing against Cyp6a9, led to the specific decrease in Cyp6a9 expression, reducing the survival rate of dsRNA-feeding larvae exposed to extreme thermal stress of 45 °C after heat hardening treatments in B. dorsalis.

CONCLUSION: This study provides insights into the evolutionary history and genetic basis of temperature adaptation in B. dorsalis.

* Title and MeSH Headings from MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine.

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